Plant Cuttings

In researching a previous post about spines, thorns, and prickles – but which mainly concerned prickles and gene-editing – I found out a lot of new-to-me facts about spines and thorns. Whilst those facts didn’t have an obvious point of inclusion in that post, I thought they were worth sharing with this blog’s audience – in the interests of increasing knowledge of these plant defences. Accordingly, here are three examples of things I learnt.

Giraffes and acacias, a thorny connection

This image, entitled “Goats in an argan tree, Morocco”, by Elena Tatiana Chis is used under the Creative Commons Attribution-Share Alike 4.0 International license.

First, I imagined that these particular pointy plant projections were an all-or-nothing phenomenon; either a plant either had them or didn’t. I wasn’t expecting to chance upon the report by AV Milewski et al. (1991) whose results imply that “increased thorn length is an induced defense”, in response to proximity of giraffes.

A little context is in order for us to appreciate what’s really going on here. For most of us who are seeking a source or two to support a statement that thorns, spines, and prickles are used by plants as a defence against the attentions of herbivores – that would like nothing better than to feast on the plant’s cells and tissues – plenty of items are available. For example, in the preceding post about CRISPR and prickle-less aubergines I cited Laura Hlusko, and items from here, here, here, and here. Those articles all supported the idea of a defensive role of thorns, spines, and prickles (which is why they were chosen). And that’s fine – in that they satisfied a requirement to state one’s sources. But, where did those sites get their evidence to make their declaration about the defensive role of various pointed structures on plant surfaces?

Looking more closely at those items, Laura Hlusko cited no sources as such, but did mention the “Phenomenal photos of thorns, prickles and spines” of the Wayne’s Word site; the two BBC and the LibreText educational items were source-free; and, although providing two references, the Learn.Genetics item from the University of Utah, only cited research articles that dealt with indirect – chemical – defences [Jörg Degenhardt, 2009], and jasmonate as a volatile molecule that acts to signal stress between plants [Abraham Koo, 2018].

At which point a reality-check – in this case some primary research into the defensive capacity of plant armature – is probably in order. Which is where Milewski et al. (1991)’s ‘giraffe paper’ comes into the story.

Milewski et al. (1991) were interested to know two things, if thorns really do act as herbivore-deterrents, and whether the presence of such armaments could be induced by herbivory. To investigate these questions they carried out a series of practical experiments. The ‘tethered goat’ study revealed that cut branches of three woody species – Acacia drepanolobium, Acacia seyal and Balanites gIabra – “that had their thorns removed suffered significantly greater herbivory by a tethered goat than did paired intact branches”.

The ‘free-range giraffes’ experiment showed that “Branches on living Acacia seyal plants that had their thorns removed suffered significantly greater herbivory by a wild population of free-ranging giraffes than did intact branches on the same plants”. Taken together, the goat and giraffe studies support the view that presence of thorns deters herbivory – in the named tree species, and for tethered goats and free-range giraffes, at least.

Additionally, Milewski et al. (1991) found that “branches [of Acacia seyal and Acacia xanthophloea] within reach of giraffes produced longer thorns and a greater density of thorns than did higher branches”, which implies that “increased thorn length is an induced defense”. Next time I write about these plant structures and defence against herbivory, I hope I remember to include this primary source to support my statements.

Warning: An introduction to aposemy

This image, captioned “Hycleus lugens, an aposematically coloured beetle” by Muhammad Mahdi Karim, is used under the terms of the GNU Free Documentation License, Version 1.2 only.

Second, the notion of ‘warning colouration’ – aposematism (Bibiana Rojas et al., 2015) – is one that we might expect to be only applicable to animals.

Indeed, it is defined as: “the advertising by an animal, whether terrestrial or marine, to potential predators that it is not worth attacking or eating” on Wikipedia’s Aposematism page*. And, on the Simple English Wikipedia Warning colouration page, we are told that “Warning coloration (or aposematism) is how animals let other animals know that they are poisonous or dangerous. It is the exact opposite of camouflage” – which at least has the benefit of presenting zoocentric consistency of definition within that universal repository of human knowledge. Additionally, the American Museum of Natural History’s article about aposematism is written only in terms of animals. As is the Encyclopaedia Britannica’s entry, with text such as “The predator, having recognized the dangerous organism as an unfavourable prey, thereupon desists from attacking it”. Finally, for good measure, undergraduates on University College, London’s BIOL2007 course’s Warning colour and mimicry lecture are told: “The function of warning colour is to deter prey [sic., presumably ‘predator’ is intended] from attacking prey that have active means of defence”. Mention of prey and predator here means this phrase is defined in purely zoological terms.

Given the considerable protective value that colours can provide in the animal kingdom, it is not unreasonable to wonder if a similar advantage might be enjoyed by plants. Well, Simcha Lev-Yadun (2001) proposed that “colorful thorns”, and those with “white spots, or white and colorful stripes” may be a botanical example of aposematic colouration. This role is presumably in addition to a physical defensive role the thorns may have. Lev-Yadun (2001) suggests that “this is a case of vegetal aposematic coloration analogous to such coloration of poisonous animals, and which communicates between plants and herbivores”.

For more on this fascinating area of enquiry, see Simcha Lev-Yadun & Moshe Inbar (2002); Simcha Lev-Yadun et al. (2002); Simcha Lev-Yadun (2003a; 2003b; 2009; 2016; 2024).

Pathogen-injecting pointy things

This image, captioned “Crataegus monogyna twig with thorns” is licensed under the Creative Commons Attribution-Share Alike 3.0 Unported license.

Third, the notion that thorns and spines might inject microbes – bacteria and fungi (and possibly viruses) – into the bodies of would-be herbivores (including humans), adding a potentially biological warfare deterrent dimension to the physical defensive role of the spiky structures.

This hypothesis was introduced by Malka Halpern et al. (2007a) thus: “Here we present evidence that thorns harbour an array of pathogenic bacteria that are much more dangerous to herbivores than the painful mechanical wounding by the thorns. Pathogenic bacteria like Clostridium  perfringens, the causative agent of the life-threatening gas gangrene, and others, were isolated and identified from date palm [Phoenix dactylifera] (with green-yellow-black aposematic spines) and ‘common hawthorn’ [Crataegus aronia] (with red aposematic thorns). These thorn-inhabiting bacteria have a considerable potential role in antiherbivory, and may have uniquely contributed to the common evolution of aposematism (warning coloration) in thorny plants”. At the end of the discussion, they conclude that “this study suggests for the first time that thorns, by wounding, insert pathogenic bacteria into the body of the herbivores as a sort of natural injection. The injury enables the bacteria to pass the animal’s first line of defences (the skin) and to cause a disease”.

Which all sounds quite scary – both for the herbivorous animals, and any humans that might come into contact with the plants’ prickly protection, particularly when they add “These bacteria potentially pose a greater risk to herbivores than that caused by the thorn injury per se” (Malka Halpern et al., 2007a). The danger to humans posed by the plant’s anti-herbivory protuberance is illustrated in this quote: “In Israel, for instance, the severity and frequency of infections following date palm thorn wounding of orchard workers has necessitated the costly practice of removal of all the millions of thorns from many of the orchards in Israel by mechanical saws” (Malka Halpern et al., 2007a)**.

Extending this notion, Malka Halpern et al. (2007b) go on to catalogue some of the bacteria found on plant pointed ‘projections’ – e.g., “aerobic and anaerobic pathogenic bacteria including Clostridium perfringens the causative agent of the life-threatening gas gangrene, Bacillus anthracis and Pantoea agglomerans [(Andrea Cruz et al., 2007)]” – and consider the medical literature which “indicates that thorns, spines or prickles also introduce pathogenic fungi into animals or humans”.

As if external surface-sited structural threats to animals aren’t bad enough, in a subsequent publication Simcha Lev-Yadun & Malka Halpern (2008) “propose that many plant species which have internal microscopic defensive sharp structures, such as raphides (calcium oxalate needles) and sharp silica bodies, may also introduce pathogenic microorganisms into the tissues of herbivores through the microscopic wounds that these defensive structures induce, especially in the mouth and digestive system.”

Having spent many years considering this phenomenon, perhaps one of the most curious ideas to have arisen from this work is the suggestion that this ‘microbe-associated ‘hypodermia’ “is actually a mutualistic [(Kaleda Denton & Dennis Krebs)] system where plants enjoy defense by microorganisms, and the microorganisms enjoy a supply of susceptible herbivorous animal targets” (Simcha Lev-Yadun & Malka Halpern, 2019).

And so we conclude our little meander into the world of spinescent plants. Fascinating structures on fascinating lifeforms, with fascinating insights into their probable, possible or putative roles in plant biology, ecology, and plants-and-people interactions.

* In fairness, much further down that Wikipedia page (and very much as an afterthought after the animal-biased interpretation of aposematism), this item does state that “Some plants are thought to employ aposematism to warn herbivores of unpalatable chemicals or physical defences such as prickled leaves or thorns”. Interestingly, although citing the work of Darrin Rubino & Brian McCarthy (2004) in support of that statement, there is no mention of any of the older work of Simcha Lev-Yadun in this regard in that Wikipedia page [although Rubino & McCarthy do cite the older work by Lev-Yadun, and Lev-Yadun does cite Rubino & McCarthy’s paper].

** Although he was probably unaware of the microbial cause of infection, one does wonder if this pointed association – of plants pricking fingers, etc. and the resulting infection – was known to noted wordsmith William Shakespeare who famously included this line in ‘the Scottish play’, “By the pricking of my thumbs, something wicked this way comes”? Maybe the play’s ‘weird sisters’ were more wise than weird?

REFERENCES

Andrea Cruz et al., 2007. Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol. 45(6): 1989-1992; doi: 10.1128/JCM.00632-07

Jörg Degenhardt, 2009. Indirect defense responses to herbivory in grasses. Plant Physiology 149(1): 96–102; https://doi.org/10.1104/pp.108.128975

Malka Halpern et al., 2007a. Plant biological warfare: thorns inject pathogenic bacteria into herbivores. Environ Microbiol. 9(3): 584-592; doi: 10.1111/j.1462-2920.2006.01174.x

Malka Halpern et al., 2007b. The potential anti-herbivory role of microorganisms on plant thorns. Plant Signaling & Behavior 2(6): 503–504; https://doi.org/10.4161/psb.2.6.4608

Abraham Koo, 2018. Metabolism of the plant hormone jasmonate: a sentinel for tissue damage and master regulator of stress response. Phytochem Rev 17: 51–80; https://doi.org/10.1007/s11101-017-9510-8

Simcha Lev-Yadun, 2001. Aposematic (warning) coloration associated with thorns in higher plants. Journal of Theoretical Biology 210(3): 385-388; doi: 10.1006/jtbi.2001.2315

Simcha Lev-Yadun, 2003a. Weapon (thorn) automimicry and mimicry of aposematic colorful thorns in plants. Journal of Theoretical Biology 224(2): 183-188; https://doi.org/10.1016/S0022-5193(03)00156-5

Simcha Lev-Yadun, 2003b. Why do some thorny plants resemble green zebras? Journal of Theoretical Biology 224(4): 483-489; https://doi.org/10.1016/S0022-5193(03)00196-6

Simcha Lev-Yadun, 2009. Aposematic (warning) coloration in plants, pp. 167-202. In: Plant-Environment Interactions. Signaling and Communication in Plants, ed. František Baluška (ed.). Springer, Berlin, Heidelberg; https://doi.org/10.1007/978-3-540-89230-4_10

Simcha Lev-Yadun, 2016. Defensive (anti-herbivory) coloration in land plants; doi: 10.1007/978-3-319-42096-7

Simcha Lev-Yadun, 2024. Visual-, olfactory-, and nectar-taste-based flower aposematism. Plants 2024, 13(3): 391; https://doi.org/10.3390/plants13030391

Simcha Lev-Yadun & Malka Halpern, 2008. External and internal spines in plants insert pathogenic microorganisms into herbivore’s tissues for defense. pp. 155-168. In: Microbial Ecology Research Trends, ed. Thijs Van Dijk.

Simcha Lev-Yadun & Malka Halpern, 2019. Extended phenotype in action. Two possible roles for silica needles in plants: not just injuring herbivores but also inserting pathogens into their tissues. Plant Signaling & Behavior 14(7): 1609858; doi: 10.1080/15592324.2019.1609858

Simcha Lev-Yadun & Moshe Inbar, 2002. Defensive ant, aphid and caterpillar mimicry in plants? Biological Journal of the Linnean Society 77(3): 393–398; https://doi.org/10.1046/j.1095-8312.2002.00132.x

Simcha Lev-Yadun et al., 2002. Colour patterns in vegetative parts of plants deserve more research attention. Trends in Plant Science 7(2): 59 – 60; doi: 10.1016/S1360-1385(01)02190-2

AV Milewski et al., 1991. Thorns as induced defenses: experimental evidence. Oecologia 86: 70–75; https://doi.org/10.1007/BF00317391

Bibiana Rojas et al., 2015. Aposematism. Current Biology 25(9): R350-R351; https://doi.org/10.1016/j.cub.2015.02.015

Darrin Darrin L Rubino & Brian C McCarthy, 2004. Presence of aposematic (warning) coloration in vascular plants of southeastern Ohio. J. Torrey Bot. Soc. 131: 252-256. 2004; https://doi.org/10.2307/4126955